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1 1 Shade coffee: update on a disappearing refuge for biodiversity 2 3 Shalene Jha 1 *, Christopher M. Bacon 2 , Stacy M. Philpott 3 , V. Ernesto Méndez 4 , Peter 4 Läderach 5 , Robert A. Rice 6 5 6 1 Integrative Biology, 401 Biological Laboratories, University of Texas, Austin, TX, USA, 7 78712; Phone: 248-719-5766, Fax: 512-232-9529, Email: [email protected] 8 9 2 Department of Environmental Studies and Sciences, Santa Clara University, 500 El Camino 10 Real, Santa Clara, California, USA, 95050-4901; Phone: Phone 408-551-3082; Email: 11 [email protected] 12 13 3 Environmental Studies Department, University of California, Santa Cruz, 1156 High Street, 14 Santa Cruz, CA, USA, 95064; Phone: 831-459-1549; Email: [email protected] 15 16 4 Agroecology and Rural Livelihoods Group (ARLG), Environmental Program and Plant and Soil 17 Science Dept., University of Vermont, The Bittersweet- 153 South Prospect St., Burlington, 18 Vermont, USA, 05401; Phone: 802-656-2539; Fax: 802-656-8015; Email: [email protected] 19 20 5 International Center for Tropical Agriculture (CIAT), Residencial San Juan de Los Robles Casa 21 #303, Apartado Postal LM-172, Managua, Nicaragua; Phone: 505-2270-9965; Fax: 505-2270- 22 9963; Email: [email protected] 23 24 6 Smithsonian Migratory Bird Center, Smithsonian Institution, Washington, D.C., USA, 20008; 25 Phone: 202-633-4209; Fax: 202-673-0040; Email: [email protected] 26 27 28

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Shade coffee: update on a disappearing refuge for biodiversity 2

3

Shalene Jha1*, Christopher M. Bacon2, Stacy M. Philpott3, V. Ernesto Méndez 4, Peter 4

Läderach5, Robert A. Rice6 5

6

1Integrative Biology, 401 Biological Laboratories, University of Texas, Austin, TX, USA, 7

78712; Phone: 248-719-5766, Fax: 512-232-9529, Email: [email protected] 8

9

2Department of Environmental Studies and Sciences, Santa Clara University, 500 El Camino 10

Real, Santa Clara, California, USA, 95050-4901; Phone: Phone 408-551-3082; Email: 11

[email protected] 12

13

3Environmental Studies Department, University of California, Santa Cruz, 1156 High Street, 14

Santa Cruz, CA, USA, 95064; Phone: 831-459-1549; Email: [email protected] 15

16

4Agroecology and Rural Livelihoods Group (ARLG), Environmental Program and Plant and Soil 17

Science Dept., University of Vermont, The Bittersweet- 153 South Prospect St., Burlington, 18

Vermont, USA, 05401; Phone: 802-656-2539; Fax: 802-656-8015; Email: [email protected] 19

20

5International Center for Tropical Agriculture (CIAT), Residencial San Juan de Los Robles Casa 21

#303, Apartado Postal LM-172, Managua, Nicaragua; Phone: 505-2270-9965; Fax: 505-2270-22

9963; Email: [email protected] 23

24

6Smithsonian Migratory Bird Center, Smithsonian Institution, Washington, D.C., USA, 20008; 25

Phone: 202-633-4209; Fax: 202-673-0040; Email: [email protected] 26

27

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In the past three decades, coffee cultivation has gained widespread attention for its critical role 29

in supporting local and global biodiversity. In this synthetic overview, we present newly 30

gathered data that summarize how global patterns in coffee distribution and shade vegetation 31

have changed and discuss implications for biodiversity, ecosystem services, and livelihoods. 32

While overall coffee area has decreased by 8% since 1990, coffee production and agricultural 33

intensification has increased in many places and shifted globally, with production expanding in 34

Asia while contracting in Africa. Ecosystem services such as pollination, pest-control, climate 35

regulation, and nutrient sequestration are generally higher in shaded coffee farms, yet many 36

coffee growing regions are removing shade trees from their management. While it is clear that 37

there are ecological and socio-economic benefits associated with shaded coffee, we expose the 38

many challenges and future research priorities needed to link sustainable coffee management 39

with sustainable livelihoods. 40

41

Keywords: agriculture, agroforestry, corridor, ecosystem services, tropical ecology 42

43

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Across the world, more than 400 billion cups of coffee are consumed per year (Illy 2002). Coffee 45

is among the most valuable legally traded commodities from the developing world (FAO 2010), 46

engaging between 14 and 25 million families in production, and millions more in the processing, 47

roasting, and selling of coffee (Donald 2004). In the last two decades, the value of shade-grown 48

(hereafter ‘shade’) coffee farms for biodiversity conservation and ecosystem service provision 49

has gained widespread attention from the public and scientific communities (De Beenhouwera et 50

al. 2013, Jha et al. 2012, Perfecto et al. 1996, Tscharntke et al. 2011). In this short time span, 51

3

global coffee distribution patterns and local coffee management practices have exhibited 52

dramatic changes, with major implications for ecology and livelihoods. In this paper, we 53

investigate trends in global coffee distributions and cultivation practices, and we review the 54

potential impacts of these geographic and management changes on biodiversity, ecosystem 55

services, resilience to climate change, and sustainable livelihoods. 56

57

1. Shifting global production patterns and management practices 58

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a. Past and current distribution of coffee 60

The two coffee species of commercial value, Coffea arabica and Coffea canephora (“robusta”), 61

both originate from Africa, with the former having generally preferred taste qualities and the 62

latter exhibiting higher yield and pest-resistance (ITC 2011, ICO 2013). C. arabica dominates 63

global coffee landscapes, accounting for 60% of all volume (ITC 2011). While coffee’s center of 64

origin lies in Ethiopia, major global dispersal of the bean occurred when Arab and European 65

traders introduced the beverage to Western Europe in the early 1500s (Ukers 1922). By the latter 66

half of the 1800s, coffee plantations of both C. arabica and C. canephora flourished throughout 67

the American tropics, and by the 1970s its cultivation dominated more than 8.8 million ha of 68

tropical landscapes. Between 1970 and 1990, global coffee area and average yields increased by 69

25% (8.8 to 11.1 million ha, and 433 to 543 kg/ha, respectively), and global production increased 70

by 58% (FAO 2010). Interestingly, although global area decreased to 10.2 million ha between 71

1990 and 2010 (the year with most recent comprehensive data), production still climbed 36%, 72

which provides evidence of overall intensification in several key countries (e.g. Brazil and 73

Colombia), coffee abandonment in others (e.g. Burundi and Kenya), as well as rapid expansion 74

4

of high-yielding coffee in new countries (e.g. Vietnam and Indonesia)(FAO 2010). Brazil, for 75

instance, saw a 112% jump in production with only a 12% increase in coffee area between 1996 76

and 2010, growth spurred by intensification that resultued in an 89% yield increase over that 77

period (FAO 2010), and recognition from coffee experts that production there has been highly 78

industrialized (Croce 2013, Izada 2013). Since the mid-1980’s, exports of “robusta” coffee have 79

increased by 92%, led by a number of Asian countries, with Vietnam being the prime example, 80

exhibiting hand-in-hand increases in both area and intensification (Guingato et al. 2008, ITC 81

2011). Robusta yields there soared from a historical average of 450 kg/ha prior to the 1950’s to 82

1558 kg/ha by 2004 (D’haeze et al. 2005), more than double the global yield average at the time, 83

revealing that a species shift alone does not explain yield increases. Given that coffee area 84

decreased globally by 9% between 1990 and 2010, whereas world production increased by 36%, 85

we posit that intensification is one of the major drivers of shifting coffee cultivation patterns. 86

A closer look reveals that the shift in production between 1990 and 2010 was regional, as 87

45% of all nations exhibiting decreases hailed from Africa, while Asian countries accounted for 88

35% of those with increased production (Fig. 1). When the first comprehensive studies of coffee 89

and biodiversity emerged in 1996, the top three producing countries were Brazil, Colombia, and 90

Indonesia. Currently, Brazil, Vietnam, and Indonesia top the list, accounting for 57% of the 8.2 91

million metric tons in 2010. In Vietnam alone, cultivated area increased by 731%, yields by 92

45%, and total production by 1102%, between 1990 and 2010 (Fig. 1). In contrast, the past 20 93

years reveal coffee area declines exceeding 20% in Ecuador, Colombia, Côte d’Ivoire, 94

Mozambique, Madagascar, Tanzania, and Rwanda (FAO 2010). 95

The contrasting and heterogeneous changes in global coffee cultivation result from 96

multiple factors, including region-specific economic development patterns, political conflict, 97

5

cultural practices, land values, wages, and labor. For example, deforestation accompanied 98

increases in coffee area in Vietnam, Indonesia, Nepal, and Panama (D’haeze et al. 2005, O’Brien 99

and Kinnaird 2003, FAO 2010). In contrast, in places where coffee area has declined, such as 100

Costa Rica and Ecuador, the expansion of high-yield agriculture has caused a decrease in coffee 101

prices, resulting in the abandonment of marginal agricultural lands (Aide and Grau 2004, FAO 102

2010), in combination with increased land prices due to urbanizaion. The result is an increase in 103

global production despite decreases in overall coffee area (Fig. 1). Higher land values due to ex-104

urbanization often displace coffee cultivation in places like Panama’s Boquete and Chiriquí 105

regions, Costa Rica, and Guatemala, areas now popular as retirement destinations (Zeltzer 2008). 106

In a number of countries, waves of political and social instability have reduced investment in 107

coffee cultivation (e.g., Rwanda, Nicaragua pre-1995, Colombia), only to have sustained global 108

prices post-2005 spur expansion in other countries (Rueda and Lambin 2013). In other regions, 109

the draw of better urban wages (e.g., Costa Rica) or displacement by other cash crops like cacao 110

(e.g., Côte d’Ivoire) has reduced the area of coffee production. 111

Despite variation in global coffee production, the majority of coffee is still produced by 112

smallholders managing fewer than 10 ha of coffee (reviewed in Jha et al. 2012), as documented 113

in Asia and Africa (e.g., Jena et al. 2012, Neilson 2008, respectively). Likewise, in Central 114

America, smallholders represent 85% of coffee producers but control only 18% of coffee 115

production lands (CEPAL 2002). In some coffee producing countries, such as Rwanda, coffee 116

farm sizes are so small that the majority of farms are measured by number of coffee trees instead 117

of hectares (e.g., 300 bushes) compared to many Mesoamerican smallholder farms, where stand 118

densities as high as 6700 coffee bushes per ha can be found (Méndez et al. 2007). These patterns 119

in farm size tend to shift depending on coffee prices and government incentives, as evidenced in 120

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Latin America, where a decrease in the number of large estates and an increase in the number of 121

smallholder and micro-producers occurred directly after the 1999 coffee crisis, when coffee 122

prices dropped to century lows (Topik et al. 2010). In the Costa Rican coffee district of Agua 123

Buena, the proportion of farmland dedicated to coffee production diminished from 52% to 24% 124

between the years 2000 and 2009, while the proportion of pasture land increased from 31% to 125

50%, largely due to basement-level international coffee prices (Babbin 2010). This example 126

highlights the need for locally and regionally specific research into the social-ecological causes 127

and consequences of changing coffee production patterns. 128

129

130

2. Vegetation management 131

In addition to global and regional shifts in coffee cultivation, within-farm vegetation 132

management has changed dramatically across centuries of coffee production. Farm-level coffee 133

management involves distinctions in elevation, sun exposure, soil conditions, density of bushes, 134

presence of additional wild or cultivated plants, age of bushes and pruning style, and 135

agrochemical use, among other factors (Moguel and Toledo 1999, Tscharntke et al. 2011). The 136

most traditional coffee growing practices, as seen in ‘rustic’ coffee, involves growing coffee 137

under a diverse canopy of native forest trees in high to moderate shade. As vegetation 138

management is ‘intensified’, plantations have fewer shade trees, fewer shade tree species, lower 139

canopy cover, and fewer epiphytes (Moguel and Toledo 1999). Shade management 140

intensification is often also accompanied by increased use of synthetic agrochemicals (e.g. 141

pesticides, fungicides, herbicides, and fertilizers). Finally, at the most ‘intensified’ end of the 142

vegetation management spectrum, coffee is grown in full sun. 143

7

Interestingly, examining coffee vegetation management across a number of countries 144

reveals that shade cover management is heterogeneous, and the changes in its global coverage 145

are region-specific. In Latin America, between 1970 and 1990, nearly 50% of all shade coffee 146

farms were converted to low shade systems (Perfecto et al. 1996). Changes varied by country, 147

ranging from 15% of farms in Mexico to 60% in Colombia (Perfecto et al. 1996). Since the 148

1990s, regions with intensively managed coffee, such as Brazil and Colombia, still remain 149

largely devoid of diverse shade systems, and have either maintained or increased areas of sun-150

coffee (Guhl 2004, Croce 2013). From the 1990s to 2010, most Latin American countries 151

decreased the percent of total coffee production area dedicated to traditional diversified shade 152

coffee production, but at a slower rate than from 1970 to the 1990s. Based on the ten countries 153

for which we have data from both the 1990s and the 2010s, we find that half of these countries 154

experienced a decrease in the percent of all coffee under traditional shade management 155

(Colombia, Costa Rica, El Salvador, Guatemala, and Nicaragua). However, because coffee 156

production areas expanded in the many of the remaining countries and several of these countries 157

reported higher percentages of shade production (e.g. Honduras, Panama), our calculations 158

suggest that there was an overall 11% increase in the area of land dedicated to diverse shade 159

coffee production. 160

However, examining at a more global scale, if we include all 19 countries for which we 161

have 2010 data, approximately 41% of coffee area is currently managed with no shade, 35% with 162

sparse shade, and only 24% with traditional diverse shade (supplemental table S1, figure 2). This 163

indicates that global shade coffee cultivation is lower than our estimates for 1996 (about 20% 164

lower), when approximately 43% of all coffee areas surveyed were cultivated in traditional 165

diverse shade. For example, between 2000 and 2009, coffee-growing regions in Costa Rica 166

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experienced a 50% loss of shaded coffee (and shade trees) in the process of conversion to sun-167

coffee, pasture, or other crops (Bosselmann 2012). The sun-coffee management style has also 168

dominated many new coffee growing regions, exemplified in Vietnam’s dramatic expansion of 169

coffee, and also evident in Thailand and Indonesia (Fig 2). In contrast, only a few countries, 170

(Colombia, Haiti, India), have continued managing diverse shade since the 1990s in all or parts 171

of their coffee regions (Fig 2). 172

Coffee vegetation management patterns are nuanced and often depend on farm size, 173

available alternatives, national and regional politics, risk aversion strategies and development 174

funding. For example, 81% of the coffee in Nicaragua and El Salvador grew under a shade 175

canopy in 1996, and while recent surveys document declines in shade tree diversity since then, 176

these declines mostly occurred on larger farms, with many smallholder cooperatives preserving 177

high levels of biodiversity, including more than 100 species of shade trees found on less than 30 178

farms (Méndez et al. 2010a). Similarly, in the Kodagu coffee-growing region of India, nearly 179

100 tree species can still be found in smallholder coffee farms (Bhagwat et al. 2005). 180

While it is clear that coffee management styles remain unevenly distributed both within 181

and among countries, the causes for this high level of variation have never been systematically 182

reviewed. We document several broad trends and posit that coffee vegetation management style 183

is influenced primarily by five main factors: 1) cultivar origin, 2) perceived resistance to disease, 184

primarily the coffee leaf rust, 3) perceived increases in yield, 4) socio-economic decisions related 185

to group membership and livelihoods, and 5) shifting economic incentives linked to global coffee 186

markets and value chains. Here, we present a comprehensive review on these five major factors 187

and document the evidence supporting and contradicting each. 188

189

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a. Cultivar origin 190

The two dominant coffee species cultivated globally are Coffea arabica (Arabica) and C. 191

canephora (Robusta), which have distinct origins and cultivation histories and thus differ in 192

flavor, ideal growing conditions, resistance to pests/pathogens, and yield, among other traits. 193

Most notably, while Arabica and its cultivars grow best at mid-high elevation (600-2000 meters), 194

exhibiting maximum photosynthetic rate at moderate temperatures and higher shade levels, 195

Robusta and its cultivars are tolerant of lower-elevation (0-800 m) and full sun exposure, 196

growing best at temperatures between 24 and 30° C (Wilson 1999). The distinctions between 197

these species, their tolerance for temperature shifts, the development of disease resistant 198

cultivars, along with a number of socioeconomic factors described in this review, underlie much 199

of the variations in current coffee vegetation management practices seen across the globe. 200

201

b. Coffee diseases and yield 202

Fungi cause most major coffee diseases (e.g., coffee leaf rust, brown eyespot, and coffee berry 203

disease), primarily affecting Coffea arabica (Staver et al. 2001), while C. canephora varieties 204

remain more resistant (FAO 2012). Coffee leaf rust (Hemileia vastatrix) is the main disease of C. 205

arabica in Latin America (Avelino et al. 2007), with the latest (2012-2013) outbreak lowering 206

harvests by 10-70% in several Latin American countries, including Peru (JNC 2013), Mexico 207

(GAIN Report, 2013), Colombia, Costa Rica, Nicaragua, Honduras, Panama, El Salvador, and 208

Guatemala (Virginio 2013). Efforts to control coffee leaf rust in the 1970s and 1980s led to much 209

of the ‘modernization’ of coffee cultivation practices in Guatemala, Honduras, Panama and other 210

countries, and include practices such as the use of supposedly disease-resistant high-yielding 211

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varieties, the reduction of shade, and the increased planting density of coffee bushes (Rice and 212

McLean 1999). 213

Although these measures were implemented to reduce coffee leaf disease, research has 214

shown that disease dynamics depend on the specific disease, local fertilization conditions, 215

humidity, elevation, temperature, and regional land management. Vegetation complexity may 216

increase coffee leaf spot (Mycena citricolor)(Avelino et al. 2007), brown eyespot (Cercospora 217

coffeicola), and coffee rust incidence, but with the latter two species, the specific cause of the 218

increase is linked to humidity, not shade, as rust incidence increases with humidity independent 219

of shade levels (Staver et al. 2001). Other studies document no correlation between shade and 220

leaf rust on Arabica varieties (e.g., Soto-Pinto et al. 2002, Lopez Bravo et al. 2012). In fact, 221

moderate shade (35-65%) can actually reduce brown eyespot (Staver et al. 2001), weeds, and the 222

citrus mealy bug, and can increase the effectiveness of parasites of other pests (Perfecto et al. 223

1996, Staver et al. 2001). Additionally, moderate shade levels can hinder fungal diseases by 224

creating windbreaks and slowing the horizontal spread of coffee leaf rust spores (e.g., Soto-Pinto 225

et al. 2002). Thus, coffee disease cannot be reduced by shade management alone, but in 226

combination with modified humidity, predator management, and local and regional landscape 227

management. 228

229

c. Shade, yield, and quality 230

The interactions between shade, yield, and ‘cup’ quality are very important to farmers, the coffee 231

industry, and consumers. Yield-focused government incentives such as Coffee Research 232

Institutes, created in the 1970s and 1980s (e.g., PROCAFE in El Salvador, ANACAFE in 233

Guatemala, ICAFE in Costa Rica, and IHCAFE in Honduras) promoted the reduction or removal 234

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of shade cover (Staver et al. 2001), created extension programs to support technified practices, 235

and financed programs that often included free or subsidized agrochemicals (Rice and McLean 236

1999). While many farmers cite increases in coffee yields as the main reason for removing shade 237

trees and native vegetation, the ecological evidence supporting decreased shade and increased 238

coffee yield is far from clear. Studies that have categorically compared yield in low vs. high 239

shade treatments have found lower yields with shade, higher yields with shade, and no 240

difference; however, studies that examine a continuous gradient of shade predominantly reveal 241

that intermediate shade levels (~35-50%) produce the highest coffee yield, likely due to the 242

balance maintained between optimal temperatures in shaded environments and optimal 243

photosynthetic rates in unshaded environments (Soto Pinto et al. 2000 and references therein). 244

While it is difficult to compare findings across studies due to geographical differences, it is clear 245

that yield is not solely or linearly linked to shade tree density or diversity. 246

Recent work also shows that cup quality is the result of a variety of interacting factors 247

that include environmental conditions, field management, adequate processing and drying, as 248

well as roasting. Surprisingly, breeding efforts for coffee have largely ignored quality and 249

focused mostly on increasing yields and disease resistance (Montagnon et al. 2012). Research 250

related to shade effects on ‘Catimor’ varieties points to shade’s positive effect on coffee bean 251

and cup quality in lower elevations (≤ 500 m) and positive to negative effects on cup quality at 252

higher elevations (Bosselmann et al. 2009). Shade appears to impart its greatest benefit in coffee 253

bean flavor for plants growing in suboptimal and heat-stressed growing regions, where shade can 254

bring environmental conditions closer to ideal levels (Muschler 2001). This suggests that shade 255

may be particularly important for maintaining coffee quality in the context of climate change, 256

especially in regions with expected temperature increases in future climate scenarios. 257

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258

d. livelihood, cooperatives, and shade coffee management 259

Farm size, cultural history, and relationship with cooperatives can influence farmer management 260

decisions and shade vegetation (Moguel and Toledo 1999). In Veracruz, Mexico, small-scale 261

producers (1-5 ha) used lower levels of agrochemicals per farm than larger scale farmers (>45 262

ha), resulting in fewer soil and water contamination problems. However, many of these small-263

scale farmers are slowly adopting several of the intensified management practices utilized by 264

larger growers (Guadarrama-Zugasti 2008). In El Salvador and Nicaragua, small (1-10 ha), 265

individually-managed farms contained higher levels of shade tree diversity compared to larger 266

(>100 ha) collectively managed holdings (Méndez et al. 2007); furthermore, tree diversification 267

levels were highest for cooperatives that clearly defined who was going to benefit from shade 268

tree products (Méndez et al. 2009). In both of these countries, individually managed farms 269

adopted vegetation diversification in order to generate a higher variety of tree products and on-270

farm benefits (Méndez et al. 2010a). These farmers managed their coffee plantations both for 271

household consumption products, as well as income from coffee. In contrast, collectively 272

managed farms focus almost entirely on producing coffee for income, due in part to the 273

challenge of distributing both the work and the benefits to obtain more on-farm products. The 274

only non-coffee product on which collective farm members are dependent and actively collect is 275

firewood; collective cooperatives have an open policy for its members to access firewood for 276

household use (Méndez et al. 2007, Méndez et al. 2009). Thus, well organized cooperatives, if 277

present, can be essential for coordinating collective action that can help smallholders manage the 278

distribution of benefits and retain land titles (Raynolds et al. 2007), potentially creating key 279

institutional environments for sustainable land stewardship. 280

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In addition to land titles, a number of assets are important for optimal livelihood: 281

participation in a cooperative or other local association, and access to land, water, loans, houses, 282

and equipment (e.g., Bacon et al. 2008). Research shows that individuals working at the 283

producing end of the coffee value chain (i.e. the farmers and countries) continue to receive a very 284

small fraction of the profits and coffee pickers and laborers (often migratory) are the most 285

marginalized actors within the coffee value chain (Oxfam 2002), since they are vulnerable to 286

shifts in production, climate, and market demands (Bacon et al. 2008, CEPAL 2002) and are paid 287

by the pound or volume of coffee cherries harvested, making as little as $2 to $10 per day in 288

many parts of the world (Oxfam 2002). For example, between 2000 and 2001, Ugandan farmers 289

received $0.14 for a kilo of unprocessed coffee that at retail would fetch more than $26.00 as 290

instant coffee in the United Kingdom (Oxfam 2002). Accounting for weight loss during the 291

processing and roasting of the coffee, this represents a 7000% price increase in the journey from 292

farm to shopping cart (Oxfam 2002). Other cases are less lopsided; Colombian farmers received 293

23-25% of the value added for coffee sold into specialty and mainstream markets in 2010 (Rueda 294

and Lambin 2013). However, while specialty coffees often result in higher prices at the farm 295

gate, questions remain about the extent to which the benefits of higher retail prices translate into 296

higher revenues for farmers and communities (Rueda and Lambin 2013). Broad-based job losses 297

in coffee farming have decreased since 2005, but seasonal hunger, marginalization, and 298

vulnerabilities persist (Bacon et al. 2008, Méndez et al. 2010b). 299

300

e. Shifting economic incentives linked to global coffee markets and value chains 301

One avenue to address declines in coffee profits and sustainable management is through the 302

specialty coffee market, which currently claims 37% of coffee volume but nearly 50% of the 303

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coffee value in the 2012 US coffee market, worth an estimated $30-32 billion dollars (SCAA 304

2012). This market has expanded rapidly in the past 20 years with estimates of total retail 305

specialty coffee sales, excluding Wal-Mart, continuing to increase in the past decade (Fig. 3). 306

The specialty coffee market supports a distinct value chain. By definition, specialty coffees 307

distinguish themselves from bulk coffee based on a variety of factors that include ‘quality’ 308

(Läderach et al. 2006), ‘sustainability’ and/or closer relationships with growers (Bacon et al. 309

2008). Within the specialty coffee market, “Sustainably certified” coffees encompass several 310

types of certifications, with Fair Trade focusing on the trade relationships, and Organic requiring 311

soil conservation and prohibiting agrochemicals and genetically modified crops, among other 312

criteria (Méndez et al. 2010b). Smithsonian’s Bird Friendly certification program has the highest 313

agro-environmental standards, requiring organic certification and more than ten species of shade 314

trees, as well as guidelines to conserve soil and water. Rainforest Alliance, Utz Certified, and 315

Fair Trade also have several agro-environmental standards restricting the use of many of the 316

most toxic pesticides and herbicides, although synthetic fertilizers and some pesticides, 317

fungicides, and herbicides are permitted. 318

A trend that has continued since the 1990s is the significant rise in the quantity of coffee 319

with one or more ecolabel. It is estimated that more than 10% of all coffees sold in 2007 carried 320

at least one sustainability certification and it is expected that this percentage will continue to 321

increase rapidly ( Giovanucci et al. 2008). In addition to the certifications previously mentioned, 322

firms, non-profit organizations, and even governments continue to partner to generate an 323

expanding number of different labels and sustainable coffee initiatives. Several key examples 324

include the Common Code for the Coffee Community (4C), and two initiatives started by large 325

coffee companies that do roasting and retailing, Starbuck’s Coffee And Farmer Equity (CAFÉ) 326

15

practices and Nestle’s Nespresso AAAA Sustainable Quality Program. These latter two 327

programs function by setting social and environmental criteria for certification and have grown 328

rapidly in the past decade, with more than 160 million pounds of coffee certified in 2006 alone 329

(Giovanucci et al. 2008). 330

A closer look at coffee profits and farmer livelihoods reveals that Fair Trade and Organic 331

certifications are able to provide a number of benefits to smallholder farmers, although 332

livelihood challenges persist (Arnould et al. 2009, Méndez et al. 2010b). For example, farmers 333

that participate in cooperatives connected to Fair Trade often have more access to credit and 334

technical support (Méndez et al. 2010b), and often receive higher prices for their coffee, 335

buffering exposure to falling coffee commodity prices and diminishing the negative 336

consequences of unexpected challenges, such as food shortages, hurricanes, and earthquakes 337

(e.g, Raynolds et al. 2007). However, Fair Trade does not necessarily improve access to food 338

through purchasing or production (Arnould et al. 2009, Méndez et al. 2010b). Furthermore, 339

although certifications are often associated with higher coffee prices, the small volumes sold and 340

additional certification costs often counterbalance added income at the household level, 341

especially as the real price premiums delivered to farmers have declined during the past decades 342

(Bacon 2010). This suggests that major changes are required to provide a strong incentive for 343

sustainable coffee management via the certification processes. 344

345

3. Biodiversity, ecosystem services, connectivity, and resilience to climate change 346

347

a. Biodiversity and ecosystem services 348

Shaded coffee plantations are increasingly valued for their contributions to biodiversity 349

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conservation and the provisioning of ecosystem services (Beenhouwer et al. 2013, Tscharntke et 350

al. 2011). Since the 1990s, shade coffee has been noted for its contributions to conserving plant, 351

arthropod, bird, bat, and non-volant mammal diversity (Perfecto et al. 1996, Donald 2004). More 352

recent studies have documented patterns of bird, ant, and tree biodiversity decline specifically in 353

response to decreasing vegetation cover and increasing management intensity (Philpott et al. 354

2008a). Biodiversity declines within coffee systems are of particular concern given that 355

ecosystem services (ES) such as pollination, pest control, erosion control, watershed 356

management, and carbon sequestration, are worth billions annually and are largely a function of 357

biodiversity levels (Wardle et al. 2011). Thus, as a whole, ecosystem services tend to decline as 358

forests are converted to shade coffee, and shade coffee is converted to low shade coffee systems 359

(Beenhouwer et al. 2013). Based on our review, more than seventy studies have directly 360

measured unique ecosystems services across varying vegetation management styles, including 361

pollination (7 studies), pest-control (42 studies), climate regulation (13 studies), and nutrient 362

cycling (10 studies). While distinct methodologies and methods of measuring response variables 363

(e.g. predator species richness vs. predator abundance) complicate meta-analyses for each unique 364

ecosystem service, we found positive effects of shade on ecosystem services in approximately 365

58% of pollination studies, 60% of the pest control studies, 100% of the climate regulation 366

studies, and 93% of the nutrient cycling studies (Table 1, Literature Search details in Table S2). 367

Specifically, vegetation complexity at the canopy level can lead to lower weed densities 368

(Beer et al. 1998) and because many shade trees fix nitrogen (e.g. Inga spp.), shade trees can 369

increase the nutrient content of soils (Beer et al. 1998). Scant shade coffee systems (1-3 tree 370

species) sequester an additional 53-55 tons of carbon per hectare in above ground biomass 371

compared to unshaded coffee monocultures (Palm et al. 2005). In Mexico, Soto-Pinto et al. 372

17

(2010) found that Inga-shaded organic coffee maintained aboveground carbon (56.9 tons C per 373

hectare) and in the soil (166 tons C per hectare) to an equal extent as nearby forests, and 374

traditional polyculture coffee maintained more carbon than all other land-use types examined 375

(Soto-Pinto et al. 2010). If we consider that scant shade systems sequester an additional 53 tons 376

of carbon per hectare (Palm et al. 2005), then the conversion of even 10% of all sun coffee 377

systems (currently covering 3.1 million ha) to even scant shade cover, would result in 1.6 billion 378

additional tons of aboveground sequestered carbon. 379

Many organisms aid in pest control in shaded farms. Ants and spiders, for example, 380

reduce damage caused by the coffee berry borer, Hypothenemus hampei Ferrari (Perfecto and 381

Vandermeer 2006) and the coffee leaf miner, Leucoptera coffeella Guer. (De la Mora et al. 382

2008). Birds and bats predate on arthropods in shaded coffee plantations. Predation services by 383

birds (Kellermann et al. 2008, Karp et al. 2013) and bats (Williams-Guillen et al. 2008) have 384

been documented to improve coffee yields by 1-14%, amounting to values that exceeded $44–385

$105/ha/year (Kellermann et al. 2008) and $75-$310/ha/year for farmers (Karp et al. 2013). 386

Pollinators are also critical for coffee production because both commercial species of coffee (C. 387

arabica and C. canephora) benefit from pollinator visits and pollinator diversity (Klein et al. 388

2003). In Costa Rica, increased fruit set due to enhanced insect pollination at a per-bush level 389

improved coffee yields by more than 20% in one 1100 ha farm, worth an estimated $62,000 390

(Ricketts et al. 2004). Again, if 10% of all sun coffee systems were converted to scant or diverse 391

shade, and if pest control services in these shaded systems continued to be valued at $75/ha 392

(Karp et al. 2013), and pollination services at $56/ha (Ricketts et al. 2004), the additional pest-393

control and pollination contributions provided could exceed $2.3 and $1.7 billion, respectively. 394

Overall, these studies highlight the great potential for increased carbon sequestration, pest-395

18

control, and pollination services within shaded coffee systems. 396

397

b. Connectivity & resilience to climate change 398

Shade coffee systems also help to connect forest fragments within the landscape mosaic. For 399

example, migratory birds often use shade coffee farms as a corridor when moving between 400

temperate and tropical regions (e.g., Greenberg et al. 1997). Pollinators such as butterflies 401

(Muriel and Kattan 2009) and native bees (Jha and Dick 2010) can migrate between forest 402

fragments and shade coffee farms. As a result, native trees support pollinators that are critical 403

during the coffee bloom and are able to maintain reproduction and gene flow processes across 404

shade coffee systems (Jha and Dick 2010). Unlike sun coffee systems, which do not provide 405

pollinators with resources throughout the year (Jha and Vandermeer 2010) and are less 406

permeable to dispersing organisms (e.g., Muriel and Kattan 2009), shade coffee farms can 407

promote pollinator populations and serve as corridors for organisms moving regionally between 408

forest fragments. 409

The importance of connectivity between coffee and protected areas is tremendous given 410

the overlap and proximity of biodiversity hotspots and coffee growing regions (Hardner and Rice 411

2002) and the importance of shaded coffee in the face of global climate change. Coffee farms are 412

often located adjacent to protected areas, and in many countries, including El Salvador, 413

Guatemala, and Costa Rica, more than 30% of area surrounding coffee regions (50 km radius) 414

fall within protected areas (Jha et al. 2012). Because organisms like birds, bats, and bees in 415

tropical habitats often disperse across short distances, the proximity of coffee farms to protected 416

areas magnifies the role of coffee in serving as an important biological corridor. 417

Shaded systems have also been identified as part of the remedy for confronting harsh new 418

19

environments in coffee regions due to climate change (DaMatta and Ramalho 2006). 419

Climatological models predict that the Caribbean and Central America will experience general 420

drying as well as stronger later-season hurricanes (Neelin et al. 2006). Hurricanes can result in 421

major economic losses to coffee farmers but farms with more complex vegetation (i.e. greater 422

tree density and tree species richness) experience significantly fewer post-hurricane landslides 423

(Philpott et al. 2008b). Coffee farmers, realizing enhanced risk in less shaded fields, have 424

engaged in post-hurricane mitigation focused on increasing the planting of more shade trees 425

within their coffee fields (Cruz-Bello et al. 2011). Shaded and diversified coffee farms also 426

provide greater climate regulating services, with potential impacts on coffee berry development 427

and overall yield (Lin et al. 2008)(Table 1). Coffee depends on seasonal rainfall (or irrigation) 428

for flowering and leaf photosynthesis, thus coffee growth rates and yields are highest at specific 429

precipitation and temperature ranges (Lin et al. 2008, and references therein). We spatially 430

quantified the change in coffee suitability in Mesoamerica using the same methodology as 431

described in Läderach et al (2010a) for Nicaragua and Schroth et al (2009) for Chiapas in 432

Mexico. We used (i) WorldClim (http://www.worldclim.org) as the current climate data base, (ii) 433

the most representative Global Climate Models (GCM) of the Fourth Assessment Report (AR4) 434

for the Special Reports on Emission Scenarios (SRES) A2a (business as usual) emission scenario 435

and (iii) existing data of coffee suitability in Central America as input data for the Maxent 436

(Phillips et al 2006) niche model. The Maxent model predicts spatially current climatically 437

suitable coffee growing areas based on presence data and the climate at these locations. The 438

established relation between the current climate and the suitability index are then projected to the 439

future. The model is based on the assumption that in the future the same climatic factors will 440

drive coffee growth as currently, therefore the model does not take into account any adaptation 441

20

strategies by means of germplasm or other improvements. We show that there is an important 442

decrease in the suitability of coffee-producing areas by 2050 (Fig. 4). Coffee suitability in this 443

context refers to areas that are climatically suitable to grow coffee, where values below zero 444

indicate areas less suitable than current conditions, and values above zero indicate areas more 445

suitable than current conditions. Specifically, the average temperature is predicted to increase by 446

2-2.5 degrees Celsius by 2050, and because coffee is very sensitive to changes in temperature, 447

coffee planting will need to move up slope by 300-400 m in order to compensate for the increase 448

in temperature (Läderach et al. 2010b). The shift in elevation will increase the pressure on forests 449

and the environmental benefits they provide to downstream communities. 450

451

4. Synthesis 452

453

Synthesizing research on global coffee distribution and cultivation practices, livelihoods, 454

biodiversity, ecosystem services, and climate resilience, it is clear that distribution and 455

cultivation practices are heterogeneous and are largely a function of local and global market 456

forces, incentives for intensification, and price premiums for diversification or improved 457

livelihoods. Traditional shade systems comprise less than 24% of the coffee areas surveyed in 458

2010, and the coffee expansion in the past two decades has been typified by intensive non-459

shaded practices. Millions of coffee farmers continue to struggle for survival despite the 460

production of high quality coffees and the generation of critical ecosystem services (Bacon et al. 461

2008). While some ecosystem services (ES) are well-known to coffee farmers (Cerdan et al. 462

2012), many others remain obscure to external agencies due to the indirect nature of their 463

services and the potential for interaction (Bennett et al. 2009). Henry et al. (2009) examined 464

21

interactions between plant biodiversity, regulating (C sequestration), and provisioning (food 465

production) ecosystem services in Kenya and found that increasing C sequestration by adding 466

more trees could have a negative effect on food production. In another example, Méndez et al. 467

(2009) showed that a higher density and diversity of shade trees resulted in a higher potential for 468

provisioning services (e.g. timber) with greater profits for farmers, but with lower coffee yields. 469

Because coffee yields are typically assessed independent of yield from timber, other crops, or 470

ecosystem services, it may be difficult for governments and conservation institutes to weigh the 471

benefits of diversified farming approaches. We propose three main focal research and 472

development areas that could advance ecosystem service provision and sustainable livelihoods in 473

coffee systems. 474

475

a. Improve certification and ecosystem service valuation 476

While certification is a common default approach used to integrate sustainable agriculture with 477

worker livelihoods, the certification approach is challenged by the limited nature of certifications 478

available and organizational and financial costs for certification. Existing certifications have 479

unique ecological standards, offer distinct economic incentives to different agents (directly to 480

growers, exporters, or to certification agencies), and also differ in the price premium provided 481

(Bacon et al. 2008, Calo and Wise 2005, Raynolds et al. 2007). As a result, farms that provide 482

substantial ecosystem services but do not qualify for existing certifications are left out, and those 483

that do qualify often face high costs of inspection and certification. For example, while Organic 484

and Fair Trade certification may raise coffee export prices (Bacon et al. 2008), these returns may 485

not cover the additional costs associated with maintenance and certification (Calo and Wise 486

2005). 487

22

We suggest research and development efforts in the exploration of a combined 488

certification approach (i.e. both Fair Trade and Organic), which could balance the costs and 489

benefits of different certification systems (Calo and Wise 2005, Philpott et al. 2007). Because 490

certification can be expensive, multiple certifications may be cost-prohibitive, especially for 491

smallholder farmers (Calo and Wise 2005), but discounts or incentives could be put into place in 492

order to minimize the costs of multiple certifications. Alternatively, government agencies could 493

subsidize or provide loans for the initial costs of certification and transition, or these expenses 494

could be paid after the first years of profit are earned. In this way and others, the certification 495

system could be revised to be more inclusive of small landholders. It is also essential that 496

certification studies incorporate an analysis of the time, labor, and economic costs involved. 497

Future work should explicitly investigate the support needed from financial, institutional, and 498

community agencies in order to successfully transition non-certified farmers to Organic, Fair 499

Trade, biodiversity- or livelihood- friendly coffees. 500

501

b. Diversify coffee farms 502

For both economic and ecological resiliency, the diversification of crops and livelihoods is 503

essential for coffee producers (Rice 2008). This review describes how a diverse array of crops 504

and shade trees provides farmers with 1) alternative income sources in cases of crop losses and 505

price fluctuations, 2) income across the growing season, 3) food for home consumption, and 4) 506

improved fertilization, erosion control, and habitat for pollinators and predators. Thus, it is 507

essential to evaluate the services and products provided by shade trees and additional crops in 508

addition to coffee yields when evaluating diversified farming approaches. An additional level of 509

diversity worth incorporating is the selection and sharing of heirloom and local seed (especially 510

23

corn, beans, rice and other subsistence crops), including local landraces which could be resistant 511

to extreme weather and changing precipitation patterns (Méndez et al. 2010a). These diversified 512

farming practices require involvement of civil society and the state in order to address the 513

structural drivers affecting persistent hunger, fraying rural safety nets for health, and educational 514

opportunities (Bacon et al. 2008). 515

516

c. Change local and global policy 517

Since 1989, the role of national governments directly influencing global coffee markets and 518

prices paid to producers (through the ICA) has decreased (Topik et al. 2010) and in these years, 519

in many regions, rural poverty rates have increased together with accelerating rates of 520

environmental destruction (Bacon et al 2008). We suggest that national governments of coffee 521

producing regions need to play a more active role in providing basic services to their populace 522

and protecting ecosystem services. Payments or Compensation for Ecosystem Services (PES) 523

provide one avenue for compensation or rewards from the beneficiaries directly to the 524

landholders and have been implemented in a number of nations, including Costa Rica, Mexico, 525

and China (reviewed in Engel et al. 2008). Rewards for ecosystem services should not be used to 526

directly regulate land management, but they could provide valuable incentives, especially with 527

the incorporation of management extension services (Engel et al. 2008, van Noordwijk and 528

Leimona 2010). The difficulties of quantifying PES or integrating them with the practices of 529

potential stakeholders or government agencies create real challenges (van Noordwijk and 530

Leimona 2010). Thus, successful programs require stakeholder involvement and development of 531

sustainable farmer livelihoods (van Noordwijk and Leimona 2010). Local, regional, and even 532

national cooperatives with administrative capacity and accountability to their membership can 533

24

leverage international development funding to improve coffee yields and quality, increase 534

production from the diversified shade canopy, and support a wide array of social development 535

projects (Raynolds et al. 2007). Incentives and infrastructure directed toward farmers who use 536

sustainable practices and preserve biodiversity could encourage producers to make a living while 537

being good stewards of the land. 538

539

8. Conclusions 540

Our findings show that while global coffee acreage has decreased since 1990, cultivation has 541

grown dramatically in Asia and has been accompanied by declining levels of diverse shade 542

coffee, thus threatening the availability and flow of ecosystem services across the globe. 543

Although there have been several gains in the growth of sustainable certifications, research also 544

suggests that livelihoods remain vulnerable and poverty and hunger are persistent in many 545

farming communities. Research in coffee systems has allowed for an improved understanding of 546

habitat management and biodiversity, a closer examination of relationships between biodiversity 547

and ecosystem services, and a greater understanding of tropical spatial ecology and connectivity. 548

Coffee has also emerged as an important test case for assessing the effects of different 549

certification programs, evaluating the links between local and global economies, and examining 550

the arena for participatory and interdisciplinary research. However, diversified efforts are needed 551

to develop effective solutions for sustainable livelihoods, and it is essential that all members in 552

the coffee value chain become active stakeholders in these efforts. From local to global scales, it 553

is clear that farmers, cooperatives, government agencies, and consumers all influence coffee land 554

management and rural livelihoods. We document that many of the landscapes that generate 555

important ecosystem services do not necessarily harvest the benefits in terms of income, 556

25

incentives, and opportunities. In order for coffee landscapes to be sustainable for humans and 557

their ecosystems, we need to 1) better incorporate human well-being and livelihoods into global 558

concepts of sustainability, 2) encourage the diversification of coffee farms to promote greater 559

resilience to changes in global markets and climates, and 3) improve the valuation and reward for 560

ecosystem services via certification and other systems in order to compensate farmers for the 561

innumerable services that shaded landscapes provide. Building synergistic and cooperative 562

relationships between farmers, certifiers, global agencies, researchers, and consumers, can 563

provide greater transparency and creative solutions for promoting ecological processes and well-564

being across global coffee systems. 565

566

Acknowledgements 567

We would like to express our gratitude to the coffee farmers of Mexico, Nicaragua, El Salvador, 568

Guatemala, Peru, Indonesia, and Costa Rica, for their support and permission to conduct research 569

with their families, in their communities, and on their land. 570

26

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789

32

Table and Figure Captions: 790

Fig. 1. Spatial distribution of global coffee cultivation. 791

792

793

33

794

Fig. 2. Percent coffee area managed beneath different technological/shade levels. Diverse shade 795

has a closed or nearly closed canopy (>40% cover) with 10 or more species of shade 796

trees, Scant shade has minimal but existing canopy (1-40% cover) and usually 1-2 species 797

of shade trees (all with <10 species), and Sun coffee has no shade or shade trees in the 798

production area. 799

800

801

802

803

34

Fig. 3. Dollar size of the specialty coffee market in Billions. 804

805

806

35

Fig. 4. Distribution of coffee suitability in 2050 and current protected areas in Mesoamerica.807

808

809

36

Table 1. Impact of increasing vegetation complexity of shade coffee on pollination, pest-control, 810

climate-regulation, and nutrient & sequestration ecosystem services (description of literature and 811

references in Table S2). 812

pollination

pest control

climate regulation

nutrient & sequestration

higher pollinator species richness1, 2

higher pollinator abundance 2, 4

higher native bee abundance, higher social bee abundance3

no impact on pollinator abundance 5

no impact on pollinator diversity 68

lower pollinator abundance 6, 68

lower pollinator species richness 68

higher parasitism 49

higher predator abundance 8,

9, 14, 16, 17, 42, 55, 56, 57, 59, 67

higher predator nest availability 11

higher predator species richness 9, 15, 42, 43, 55, 67

higher removal of pests 7, 12, 13,

44, 46, 47, 53, 58

lower pest abundance 10, 13, 48,

51, 52, 61, 62, 63, 64

lower pest damage 66 0 no impact on pest abundance

61, 62, 63 0 no impact on predator

abundance 15, 16, 18, 49, 64, 65 0 no impact on predator species

richness 49, 54 0 no impact on prey abundance

50 0 no impact on removal of pests

42, 43, 45

higher pest abundance 19, 20, 21,

22, 51, 53

higher pest species richness 60

lower predator abundance 17,

65

lower predator species richness 57

higher leaf wetness frequency 19

lower air, soil, or leaf temperatures (mean maximum or mean) 23, 25,

27, 28, 29, 30, 33

lower global, PAR, or net solar radiation 23, 25, 28, 30,

33

fewer and smaller landslides 24

lower wind speed 25, 28, 30

lower soil evaporation rates, lower plant evaporative transpiration 26

higher relative extractable water in soil, higher soil moisture 29, 31,

33

higher precipitation capture 31

lower humidity and solar radiation fluctuations 32

lower frost damage 34

lower intra-day fluctuations in temperature, lower rate of cooling of night air 19,

32, 33

higher above ground carbon storage 35, 38,

39, 69

higher total soil organic C 27, 69

higher N mineralization, lower NP nutrient excess (inputs minus outputs) 27, 36, 41

higher soil microbial activity 27

higher soil pH, CEC, Ca, and Mg, and lower K 37

higher N concentration in leaves 38

higher fractions of P available to agricultural crops 40

no impact on soil organic carbon 70

813